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An Endemic Plant and the Plant-Insect Visitor Network of a Dune Ecosystem

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An Endemic Plant and the Plant-Insect Visitor Network of a Dune Ecosystem Global Ecology and Conservation 18 (2019) e00603 Contents lists available at ScienceDirect Global Ecology and Conservation journal homepage: http://www.elsevier.com/locate/gecco Original Research Article An endemic plant and the plant-insect visitor network of a dune ecosystem * Claudia L. Jolls a, c, d, , Jaclyn N. Inkster a, b, Brian G. Scholtens c, e, Pati Vitt d, f, Kayri Havens d a Department of Biology, Howell Science Complex MS 551, East Carolina University, Greenville, NC, USA b Nomad Ecology LLC, Martinez, CA, USA c University of Michigan Biological Station, Pellston, MI, USA d Chicago Botanic Garden, Glencoe, IL, USA e College of Charleston, Charleston, SC, USA f Lake County Forest Preserves, Libertyville, IL, USA article info abstract Article history: Network theory increasingly is used to quantify and evaluate mutualistic interactions, such Received 14 November 2018 as those among plants and their flower-visiting insects or pollinators. Some plant species Received in revised form 26 March 2019 have been shown to be important in community structure using network metrics; how- Accepted 26 March 2019 ever, the roles of plant taxa, particularly rare species, are not well understood. Pitcher's thistle (Cirsium pitcheri), a threatened endemic of Great Lakes shorelines, flowers late-June Keywords: to early-August, when other floral resources may be less abundant or unavailable. We Plant-insect visitor network performed 10 min insect visitor observations on all insect pollinated plants in 44e10 m by Cirsium pitcheri fl Rarity 10 m plots at Sturgeon Bay, northern lower MI, USA, during C. pitcheri owering and fl Dune endemics recorded plant species, number of open owers, species of insect visiting, and number of visits by insects. Pitcher's thistle received 18.2% of all 600 recorded visits, 61.1% more than the next most visited plant. Pitcher's thistle also received visits from 22 of the 59 different insect species in the network, twice as many as the next most visited plant species. Species-level network analysis metrics showed that Pitcher's thistle was most generalized, with greatest species strength, betweenness, and connectance scores of any other plant taxon, demonstrating network topological importance. Pitcher's thistle received signifi- cantly more insect visits relative to its abundance that did any other plant species. Therefore, conservation of C. pitcheri and of other rare taxa, particularly in xeric and low diversity systems, can be significant beyond species-level management and may extend to conservation of the plant-insect community. © 2019 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). 1. Introduction A plant-pollinator (or plant-insect visitor) network is defined as the cumulative interactions between plants and their animal visitors (potential pollinators) in an ecosystem. Network analysis has been used to assess the topological importance, or the level of support in network stability, of individual species within ecological networks (Jordan et al., 2008). Such * Corresponding author. Department of Biology, Howell Science Complex MS 551, East Carolina University, Greenville, NC, USA E-mail address: [email protected] (C.L. Jolls). https://doi.org/10.1016/j.gecco.2019.e00603 2351-9894/© 2019 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/ licenses/by-nc-nd/4.0/). 2 C.L. Jolls et al. / Global Ecology and Conservation 18 (2019) e00603 networks focus on multi-way interactions within conventional food webs, i.e., gathering of food resources, not just the one- way transfer of pollen and resultant seed set (pollination). Also, confirmation of effective pollination is not always possible. Insect visitation to flowers is more often observed and such interactions are termed “plant-flower visitor” or “plant-insect visitor” networks (e.g., Koski et al., 2015, conventions we adopt here). Flowering plants that attract a wide variety of visitors (several orders of insect or animal) are considered generalists, as opposed to specialists, which attract few visitors (one order of insect or a few specific species) (Waser et al., 1996). Plants are considered generalists based not only on the number of visiting insect species, but also on the number of visits of each interaction relative to the rest of the network (Blüthgen et al., 2006; Sahli and Conner, 2006). The extinction of highly connected species has the potential to result in a cascade of secondary extinctions of species, including loss of generalist pollinators such as Hymenoptera and Lepidoptera, and ultimately imperil pollination networks (Memmott et al., 2004). A keystone species was originally defined as a predator species that holds other species in check that would otherwise dominate the system (Paine, 1969). Recent usage of the keystone concept has been extended to refer to a species whose effect is disproportionately large in relation to body size and abundance (Power et al., 1996). While the term is beset by ambiguities and controversy, the concept may be useful in its application in conservation (Mills et al., 1993). This concept has been applied to plant-flower visiting insect interactions (keystone host mutualists) by analyzing the number of connections and the strength of those connections to other species (Martín Gonzales, 2010; Pocock et al., 2011). Other species-level metrics (connectedness, betweenness, measures of species generality or specificity, and species strength) have been used to identify potentially important plants in plant-insect networks (Martín Gonzales, 2010; Pocock et al., 2011; Robson, 2014; Koski et al., 2015). Even rare plants, those with limited geographic distribution, local abundance, and habitat specificity (Rabinowitz, 1981), can be important members of flower-insect visitor networks (Memmott et al., 2004; Severns and Moldenke, 2010). Rare endemic plants of oceanic island networks can have higher linkage to pollinators than do non-endemics and robustness of this network (ability to withstand perturbation) can be partially attributed to the presence of native plant species (Olesen et al., 2002). Similarly, a rare clover endemic to the sand dunes of Manitoba and Saskatchewan (Dalea villosa var. villosa (Nutt.) Spreng., Fabaceae) is an important nectar and pollen resource for insects, with significantly higher visitation rates than all the other plant species present (Robson, 2014). Rare species, particularly in low diversity communities such as dunes, similarly may have major roles in plant-flower visitor networks. Although identification of “keystone” taxa is best confirmed through removal of these species followed by quantification of community response, this is rarely possible with protected taxa or those with intractable life histories (large size, long-lived, slow-growing). Network analysis of plant-flower visitor interactions is particularly useful for these rare species and their contributions to ecosystem function (Mouillot et al., 2013; Leitao et al., 2016). Pitcher's thistle (Cirsium pitcheri (Torr.) Torr. & A. Gray, Asteraceae) is a federally threatened species, endemic to the sand dunes and cobble shores of the western Great Lakes. This herbaceous perennial grows for 4e8 yr as a vegetative rosette. In its last year of life, the plant bolts, flowers, producing approximately 30 floral heads per plant on average (Havens et al., 2012; Inkster, 2016) before it sets seed and then dies (monocarpic). Pitcher's thistle has no means of vegetative reproduction and relies solely on seed set for reproduction. Bagged inflorescences (heads or capitula) do produce seed, confirming potential for self-pollination within a head in the absence of an insect visit (autogamy). However, insect transfer of pollen is important for seed set, as is true for many Asteraceae. Selfing can occur via pollinator movements within and among heads on the same plant (geitonogamy), but more seeds per head are produced with insect-mediated outcrossing (Loveless, 1984). Pitcher's thistle flowers from late June to early August, a long (2 mo) period, when other floral resources in the dune ecosystem may not be present or as abundant (Voss and Reznicek, 2012; Goodwillie and Jolls, 2014). Fig. 1 presents flowering phenology for plant species co-occurring with Pitcher's thistle for which flowering period is well-documented. This flowering plant is primarily pollinated by members of the genus Bombus and the bee family Halictidae, but visits from other solitary Fig. 1. Phenology of flowering periods of Great Lakes dune insect pollinated plant species. Flowering period data are from floras (Voss, 1972; Ownbey and Morley, 1991; Flora of North America Editorial Committee, 1993; Chadde, 2013). Width of the box for each species reflects the length of flowering season. C.L. Jolls et al. / Global Ecology and Conservation 18 (2019) e00603 3 bees, butterflies, flies and beetles have also been documented (Keddy and Keddy, 1984; Loveless, 1984; Baskett et al., 2011). This diversity of insect visitors suggests C. pitcheri may be a generalist and could function as an important floral resource in the Great Lakes natural dune ecosystem. Although this plant is threatened and limited in its distribution, we hypothesized that C. pitcheri is a valuable floral resource to the insect fauna of the local dune ecosystem during its flowering period. 2. Materials and methods 2.1. Field study We observed insect visitation on all insect-pollinated flowering plants in randomly selected plots at Sturgeon Bay, Wil- derness State Park, Emmett County, northwestern lower MI. The site is a large west-facing complex of parallel beach-dune ridge complex on the east shore of Lake Michigan (Lichter, 1998). Sturgeon Bay suffers comparatively minimal negative impacts from human use of the coastal shoreline. Floral diversity is higher than neighboring sites. Pitcher's thistle populations here are relatively large, associated with the primary and secondary dunes near the lake, characterized by strong winds, sand erosion and deposition, low organic matter, and low vegetation cover.
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